Studies have shown that morbidity and mortality rates due to cancer among recent immigrants are lower than those among the native-born population. The objectives of this study were to describe the incidence of colorectal and breast cancer among immigrants from major regions of the world compared to Canadian-born residents of the province of Ontario and to examine the role of length of stay and neighborhood income.
Trang 1R E S E A R C H A R T I C L E Open Access
Incidence of breast and colorectal cancer
among immigrants in Ontario, Canada:
a retrospective cohort study from 2004-2014
Jennifer Shuldiner1*, Ying Liu2and Aisha Lofters3
Abstract
Background: Studies have shown that morbidity and mortality rates due to cancer among recent immigrants are lower than those among the native-born population The objectives of this study were to describe the incidence of colorectal and breast cancer among immigrants from major regions of the world compared to Canadian-born residents of the province of Ontario and to examine the role of length of stay and neighborhood income
Methods: Retrospective cohort study including all individuals 18 years and over residing in Ontario from 2004 to
2014 Age-standardized incidence rates (ASIR) were calculated for immigrants from each world region versus
Canadian-born residents and stratified by neighborhood income quintile and length of stay Binomial regression analysis was used to determine the association of neighbourhood income, length of stay, and location of birth with colorectal and breast cancer incidence
Results: Canadian immigrants born in South Asia had the lowest colorectal and breast cancer incidence (colorectal: women: ASIR = 0.14; men: ASIR = 0.18; breast: ASIR = 1.00) compared to long-term residents during the study period (colorectal: women: ASIR = 57; men: ASIR = 72; breast cancer ASIR = 1.61) In multivariate analyses, neighboorhood income did not consistently play a significant role in colorectal cancer incidence; however higher neighbourhood income was a risk factor for breast cancer among immigrant women (adjusted relative risk for highest
neighboorhood income quintile versus lowest income quintile =1.21, 95% CI = 1.18–1.24) Increased length of stay was associated with higher risk of cancer After adjusting for age, neighborhood income, and length of stay, those born in Europe and Central Asia had the highest risk of colorectal cancer compared to those born in East Asia and Pacific and those born in the Middle East had the greatest additional risk of breast cancer
Conclusions: After correcting for age, breast and colorectal cancer incidence rates among immigrants differ
according to their region of birth and recent immigrants to Ontario have lower colorectal and breast cancer
incidence rates than their native-born peers However, those advantages diminish over time These findings call for Ontario to generate tools and interventions to maintain the health of the immigrant population, particularly for those groups with a higher incidence of cancer
Keywords: Immigrant, Cancer incidence, Standardized incidence ratio, Breast cancer, Colorectal cancer
* Correspondence: Jennifer.shuldiner@mail.utoronto.ca
1 University of Toronto, 155 College Street, Toronto, ON M5T 1P8, Canada
Full list of author information is available at the end of the article
© The Author(s) 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/ ), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made The Creative Commons Public Domain Dedication waiver
Trang 2Immigrants represent a large, increasing and vital
segment of the Canadian population Most Canadian
studies have shown that morbidity and mortality rates of
chronic disease among recent immigrants are lower than
those among the general Canadian population
suggest-ing that immigrants enjoy the“healthy immigrant effect”
whereby they are in better physical condition on arrival
than host country inhabitants as a result of selective
migration [1–4]
Ontario, the largest province in Canada, has a large
and diverse immigrant population and approximately
one-third of the population in Ontario is foreign-born
[5] Ontario also has a provincial cancer registry that
includes data on all residents diagnosed with cancer
and universal public health care coverage, thus
mak-ing it an ideal location to explore cancer incidence
among immigrants at the population level However,
there has been little recent research examining cancer
incidence in the immigrant population [6]
Colorectal cancer is the third most common cancer
diagnosed in men and women with 26,800 cases per
year in Ontario Breast cancer is the most common
cancer among women with 26,300 cases a year in
clear provincial screening guidelines and are often
There-fore, the overall objective of this study was to
exam-ine how the incidence of colorectal and breast cancer
among immigrants from major regions of the world
compare to Canadian-born residents of Ontario We
also explored the roles of age, gender, socioeconomic
status and time in Canada
Methods
The following datasets were linked using unique
encoded identifiers and analyzed at the Institute for
Clinical Evaluative Sciences (ICES) The Registered
Persons Database was used to identify people aged
18 years and over in the province of Ontario eligible
for health care The Registered Persons Database
contains basic demographic information for those
who have ever received an Ontario health card
num-ber for the province’s universal health care system
(overall linkage rate = 96.5%) All citizens and
per-manent residents are eligible for health care The
second database was the Immigration Refugee and
in-cludes individuals who have landed immigrant or
permanent resident status at any time from 1985 to
2014 Immigrants were defined as those identified in
the IRCC Database, and long-term residents were
(Canadian-born and immigrants who arrived before
1985) The IRCC database was also used to identify country of birth, and countries were further col-lapsed into eight regions, broadly defined according
to the World Bank classification (1, Caribbean and Latin America; 2, East Asia and Pacific; 3, Eastern Europe and Central Asia; 4, Middle East and North Africa; 5, South Asia; 6, Sub- Saharan Africa; 7, USA, Australia, and New Zealand; and 8, Western Europe) Third, we identified incident breast and colorectal cancer cases by linking the cohort to the Ontario Cancer Registry from 2004 to 2014 The Ontario Cancer Registry is a passive surveillance pa-tient registry that links data from hospitals, cancer centers and pathology laboratories; incidence data has been previously assessed as having approximately
standard
Covariates
Using the postal-code conversion file [11], ecological-level measures of income status were estimated using data from the 1996, 2001 and 2006 Canadian census and applied to individual cases according to the dissemin-ation area where the individual resided Dissemindissemin-ation areas are the smallest geographic census unit for which census data are available, and are uniform in population size, which is targeted from 400 to 700 persons Individ-uals were then grouped into income quintiles ranging from 1 (20% lowest income) to 5 (20% highest income) Length of stay was measured by calculating the time since immigration until December 31, 2014 or cancer incidence
Analysis
The age-standardized annual incidence rates (ASIR) were calculated using the 2010 Canadian population
as standard, for long-term residents, for immigrants, and then by world region of origin for immigrants
To assess the effect of neighboorhood income and length of stay in Canada, ASIR were stratified by time since immigration 0–5 years, 6–10 years and 11+
through 5)
Predictors of breast and colorectal cancer incidence among all residents in Ontario, 2004–2014 were assessed by two binomial regression models, one among the entire cohort and one among only immi-grants Among the entire cohort, predictors entered into the model included age, place of birth and neighborhood income quintile The second model cal-culated among only immigrants assessed the effect of age, neighborhood income quintile, length of stay and region of birth The analyses produced adjusted rate
Trang 3ratios (RR) with corresponding confidence intervals
(CI) Statistical significance was determined at the 0
05 level All analyses were conducted using SAS
stat-istical software, version 9.4 This study was approved
by the institutional review board at Sunnybrook
Health Sciences Centre, Toronto, Canada
Results
Demographic characteristics of the study population
than long-term residents on average: mean age
ranged from 40.2 ± 13.7 for Sub-Saharan Africa to
44.7 ± 15.8 for East Asia and Pacific, whereas
were born in the Middle East and North Africa had
spent the least amount of time in Canada on
aver-age (10.7 ± 6.0 years), and those born in Europe and
Central Asia had spent the longest amount of time
(14.2 ± 6.9) Sub-Saharan Africa, followed by Latin
America and the Caribbean, had the greatest
per-centage of immigrants living in the lowest income
quintile (Table 1)
Place of birth
Age-standardized incidence rates varied by region,
with long-term residents consistently having the
highest rates and South Asian immigrants
consist-ently having the lowest rates of colorectal and breast
colorectal cancer was highest among Europe and
Central Asia for men (ASIR = 0.65) and females
of Canada, the highest ASIR for breast cancer was among those from Middle East and North Africa (ASIR = 1.49, Fig 1)
Length of stay and income
ASIR were also examined based on length of stay and neighborhood income quintile We found that the ASIR were not associated with neighborhood income quintile for females and males with colorectal cancer
breast cancer increased for higher neighborhood in-come quintiles for those born in Europe and Central Asia, South Asia, Sub-Saharan Africa, and New Zea-land, Australia and the United States, but did not
were no clear patterns seen for length of stay for both colorectal and breast cancer in the descriptive analysis and advantages enjoyed by immigrants ap-peared to disappear after spending over 10 years in Canada for both colorectal and breast cancer inci-dence (not shown)
In the binomial regression analysis among both long-term residents and immigrants we found that, after controlling for age and neighborhood income, immigrants enjoyed a healthy immigrant effect and were at lower risk of breast and colorectal cancer
colo-rectal cancer, those in the highest neighborhood
Table 1 Demographic characteristics of long-term residents and immigrants in the study population
Characteristic Long-term
residents
East Asia and Pacific
Europe and Central Asia
Latin America and the Caribbean
Middle East and North Africa
South Asia Sub-Saharan
Africa
US, New Zealand and Australia
N = 94,136,709 N = 5,235,458 N = 3,789,083 N = 2,718,788 N = 1,844,075 N = 4,613,474 N = 1,141,050 N = 380,564 Sex (%)
Age (years)
Neighborhood income quintile (%)
Length of stay
(years) (%)
Mean (SD)
Trang 4income quintile had a lower risk of incident cancer
compared to those in the lowest neighborhood
in-come quintile for both men (RR = 0.96, 95% CI = 0
93–0.99) and women (RR = 0.95, 95% CI = 0.92–0.99)
Also, a significant (p < 0.01) trend was found for
in-come for colorectal cancer where risk was higher
among those in lower income neighborhoods The
effect of neighborhood income on the risk of breast
cancer for women was in the opposite direction with
each neighborhood income quintile conferring
add-itional risk of breast cancer (RR = 1.21 for Q5 versus
Q1, CI = 1.18–1.24), and this relationship was
signifi-cant as a trend as well (p < 0.0001) After adjusting
for age and neighborhood income, those born in
Europe and Central Asia had the greatest additional
risk of colorectal cancer compared to long-term
resi-dents Regarding breast cancer, those born in the
Middle East and North Africa had the greatest
additional risk of colorectal cancer compared to long-term residents Those born in South Asia had the lowest rates of breast and colorectal cancer
In binomial regression analysis among immigrants only, when controlling for age, neighborhood in-come, and place of birth, we found that the risk of colorectal and breast cancer increased for each add-itional five years that immigrants lived in Canada
risk of breast cancer where risk increased 7% for each additional five years in Canada (p < 0.0001) After adjusting for age, neighborhood income, and length of stay, those born in Europe and Central Asia had the greatest additional risk of colorectal cancer compared to the reference group for this ana-lysis of those born in East Asia and the Pacific Those born in South Asia had the lowest risk for
Age standardized incidence rates per 1000 for females with colorectal cancer, 2004-2014
Age standardized incidence rates per 1000 for males with colorectal cancer, 2004-2014
Age standardized incidence rates per 1000 for females with breast cancer, 2004-2014
0.57 0.37
0.51 0.32
0.31 0.14
0.24 0.27
Long-term resident East Asia and Pacific Europe and Central Asia Latin America and the Caribbean Middle East and North Africa
South Asia Sub-Saharan Africa
US, NZ and Australia
Age standardized incidence rate
0.72 0.44
0.65 0.30
0.38 0.18
0.41 0.34
Long-term resident East Asia and Pacific Europe and Central Asia Latin America and the Caribbean Middle East and North Africa
South Asia Sub-Saharan Africa
US, NZ and Australia
Age standardized incidence rate
1.61 1.07
1.35 1.09
1.49 1.00
1.14 1.30
0.00 0.20 0.40 0.60 0.80 1.00 1.20 1.40 1.60 1.80 Long-term resident
East Asia and Pacific Europe and Central Asia Latin America and the Caribbean Middle East and North Africa
South Asia Sub-Saharan Africa
US, NZ and Australia
Age standardized incidence rate
a
b
c
Figure 1 a: Age standardized incidence rates per 1000 for females with colorectal cancer, 2004 –2014 b: Age standardized incidence rates per
1000 for males with colorectal cancer, 2004 –2014 c: Age standardized incidence rates per 1000 for females with breast cancer, 2004–2014
Trang 5colorectal cancer among males and females and of
breast cancer compared to those born in East Asia
and the Pacific (Table 3)
Discussion
Our results demonstrate several important findings
regarding immigrant health and cancer incidence in
Ontario First, our multivariate regression analyses showed that the healthy immigrant effect exists for recent immigrant arrivals for breast and colorectal cancer incidence but that it dissipated with time and each year in Canada is associated with a 5–7% increase in risk Second, our study demonstrated that place of birth was an important predictor, with
Age standardized incidence rates per neighborhood income quintilefor females with colorectal cancer, 2004-2014
Age standardized incidence rates perneighborhoodincome quintilefor males with colorectal cancer, 2004-2014
0 0.5 1 1.5 2 2.5
Income quintile
East Asia and Pacific Europe and Central Asia Latin America and the Caribbean
US, NZ and Australia
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8
Income quintile
East Asia and Pacific Europe and Central Asia Latin America and the Caribbean Middle East and North Africa South Asia Sub-Saharan Africa
US, NZ and Australia
Age standardized incidence rates per neighborhood income quintilefor females with breast cancer, 2004-2014
0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 1.8
Income quintile
East Asia and Pacific Europe and Central Asia Latin America and the Caribbean Middle East and North Africa South Asia Sub-Saharan Africa
US, NZ and Australia
a
b
c
Figure 2 a: Age- standardized incidence rates per neighborhood income quintile for female colorectal cancer, 2004 –2014 b: Age- standardized incidence rates per neighborhood income quintile for male colorectal cancer, 2004 –2014 c: Age- standardized incidence rates per neighborhood income quintile for female breast cancer, 2004 –2014
Trang 6Table 2 Multivariate model for entire cohort by cancer site Variables included in the model are age, sex (for colorectal cancer), income and region of birth
p-value
Income
Place of birth
Income
Place of birth
Income
Place of birth
Trang 7those from Europe and Central Asia being at
high-est risk among immigrants of developing colorectal
cancer (incidence among men = 65 and females =0
51) and those from South Asia having the lowest
rates (females = 0.14 and males = 0.18) Those from
the Middle East and North Africa were at highest
risk among immigrant women to develop breast
can-cer (incidence = 1.49) and those from South Asia were
the lowest (incidence- = 1.00) Third, we saw that
neighborhood income did not play a role in colorectal
cancer incidence but that higher neighborhood
in-come was a risk factor for breast cancer incidence
among immigrant women (RR = 1.21 95% CI = 1.18, 1
24)
Upon examining place of birth, we saw large
dif-ferences (49–264% difference) in age standardized
rates between places of birth In comparison to
long-term residents the largest differences were for
those born in South Asia who had the lowest rates
for colorectal and breast cancer These differences
are most likely attributed to differences in their
home countries where South Asia has among the
lowest incidence rates compared to other regions for
incidence rates for United States, New Zealand and
Australia were lower for breast and colorectal cancer
com-pared to long-term immigrants This was surprising, as
Canada is considered to be a historically high-risk area for
colorectal and breast cancer, similar New Zealand, United
States and Canada, reflecting similar dietary and lifestyle
factors [13]
Neighborhood income did not play a significant
role in colorectal cancer incidence Those in the
highest neighborhood income quintile had slightly
lower rates of colorectal cancer in the regression
model including all Ontario residents; however, no
effect was seen when examining rates among only
immigrants In contrast, we saw that higher
neigh-borhood income was a risk factor for breast cancer
incidence, both unadjusted and in regression models
Similarly, Canadian and American data have shown that women in neighborhoods with higher neighbor-hood incomes have a higher risk of developing breast cancer [14, 15]
An important dimension of the healthy immigrant effect is that the immigrant advantage we found ap-peared to disappear after spending over 10 years in Canada for both colorectal and breast cancer inci-dence In addition, in the regression model limited
to immigrants we saw that risk of cancer increases (5–7%) for each additional five years in Canada for both colorectal and breast cancer Similarly, re-searchers have previously found that among Ontar-ian immigrants, despite the original advantage with immigration, there is a steady decline in survival,
Ana-lysis of Statistics Canada’s Longitudinal Survey of Immigrants to Canada showed a decline in self-assessed health, physical health, and mental health among immigrants as little as two years after arrival
health outcomes may stem from the process of ac-culturation where immigrants begin to take on Canadian habits such as smoking, alcohol
data from representative surveys have shown that immigrants did not show higher rates of daily smoking initiation, however, they were much more likely than the Canadian-born population to have had a substantial weight gain since immigrating
unlikely that they are responsible for changes in in-cidence occurring over the short time observed in this study
Others maintain that worsening of health status is due to barriers to health services including lack of familiarity with the Canadian health system and
the underuse of preventative health screening and
Table 2 Multivariate model for entire cohort by cancer site Variables included in the model are age, sex (for colorectal cancer), income and region of birth (Continued)
p-value
a
Binomial regression model
b
per 5 years
*
P value of trend p < 0.005
Bold values are <0.05
Trang 8Table 3 Multivariate model for immigrant cohort by cancer site Variables included in the model are age, sex (for colorectal cancer), income, region of birth and length of stay
Income
Place of birth
Income
Place of birth
Income
Place of birth
Trang 9disparities in cervical and breast cancer screening for
foreign-born women have long been documented in
shown that cancer incidence may increase in the
first decade after immigration and it reaches the
population level in the host country in 1–2
genera-tions [27, 28]
This large cohort study has examined cancer
inci-dence among immigrants in Canada which has not
databases, universal health care and excellent
link-age we could consider the effects of region of birth,
neighborhood income and length of stay However,
there are several limitations that should be noted
We were not able to determine if this was a cohort
effect where those that immigrated more recently
were healthier than those who immigrated over ten
years ago Our analyses used the
world-region-of-birth; this method of grouping could be problematic
as countries within any region are not
income-related information, we linked residential
postal codes to neighborhood -level income which
in rural areas, however, according to our data 99%
of all immigrants to Canada settle in urban areas
Additionally, immigrants may have lived in other
countries other than their country of birth before
they came to Canada, thus possibly reducing the
significance of birthplace as a determinant Finally,
our analysis was not able to account for risk factors
such as behaviour (i.e smoking and alcohol) and
stress for cancer
Conclusions
Our analysis showed breast and colorectal cancer
in-cidence rates among immigrants to Ontario, Canada
are lower than residents and these rates differ
accord-ing to region of birth, however, those advantages
diminish after arrival Results from this hypothesis-generating research initiative hold significant immigra-tion and health policy implicaimmigra-tions, and add further intricacy to the study of the social determinants of health The results call for Ontario to generate tools and interventions to maintain the health of immigrant population
Abbreviations ASIR: age-standardized incidence rates; CI: Confidence Intervals; RR: Rate ratios
Funding This study is supported by the Institute for Clinical Evaluative Sciences, which
is funded by an annual grant from the Ontario Ministry of Health and Long-Term Care The opinions, results, and conclusions reported in this paper are those of the authors and are independent from the funding sources No endorsement by the Institute for Clinical Evaluative Sciences or the Ontario Ministry of Health and Long-Term Care is intended or should be inferred Parts of this material are based on data and information provided by Cancer Care Ontario (CCO) The opinions, results, views, and conclusions reported in this paper are those of the authors and do not necessarily reflect those of CCO No endorsement by CCO is intended or should be inferred All inferences, opinions, and conclusions drawn in this paper are those of the authors, and do not reflect the opinions or policies of the data stewards Immigration data was obtained from the Immigration, Refugees and Citizenship Canada database held at the Institute for Clinical Evaluative Sciences Aisha Lofters is supported by a New Investigator Award from the Canadian Institutes of Health Research and as a Clinician Scientist by the University of Toronto Department of Family & Community Medicine This study was funded by a Career Development Award in Cancer Prevention from the Canadian Cancer Society Research Institute (Aisha Lofters).
Availability of data and materials The data that support the findings of this study are available from the Institute for Clinical Evaluative Sciences of but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available Data are however available from the authors upon reasonable request and with permission of Institute for Clinical Evaluative Sciences.
Authors ’ contributions J.S: Conceptualization of study, data interpretation and preparation of manuscript A.L: Conceptualization of study, data interpretation and manuscript review L.Y.: Statistical analysis and manuscript review All authors read and approved the final manuscript.
Table 3 Multivariate model for immigrant cohort by cancer site Variables included in the model are age, sex (for colorectal cancer), income, region of birth and length of stay (Continued)
a
per 5 years
b
binomial regression models
* P value of trend p < 0.005
Bold values are <0.05
Trang 10Ethics approval and consent to participate
This study was approved by the institutional review board at Sunnybrook
Health Sciences Centre, Toronto, Canada It contains deidentified data, and
therefore consent was waived by the institutional review board.
Competing interests
The authors declare that they have no completing interest.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
Author details
1 University of Toronto, 155 College Street, Toronto, ON M5T 1P8, Canada.
2 Institute for Clinical Evaluative Sciences, 2075 Bayview Ave, Toronto, ON
M4N 3M5, Canada.3Li Ka Shing Knowledge Institute, 209 Victoria St, Toronto,
ON M5B 1T8, Canada.
Received: 9 February 2018 Accepted: 26 April 2018
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